Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1981 Aug 1;90(2):279–288. doi: 10.1083/jcb.90.2.279

Regulation of the higher-order structure of chromatin by histones H1 and H5

PMCID: PMC2111872  PMID: 7287811

Abstract

Chicken erythrocyte chromatins containing a single species of linker histone, H1 or H5, have been prepared, using reassembly techniques developed previously. The reconstituted complexes possess the conformation of native chicken erythrocyte chromatin, as judged by chemical and structural criteria; saturation is reached when two molecules of linker histone are bound per nucleosome, as in native erythrocyte chromatin, which the resulting material resembles in its appearance in the electron microscope and quantitatively in its linear condensation factor relative to free DNA. The periodicity of micrococcal nuclease-sensitive sites in the linker regions associated with histone H1 or H5 is 10.4 base pairs, suggesting that the spatial organization of the linker region in the higher-order structure of chromatin is similar to that in isolated nucleosomes. The susceptible sites are cut at differing frequencies, as previously found for the nucleosome cores, leading to a characteristic distribution of intensities in the digests. The scission frequency of sites in the linker DNA depends additionally on the identity of the linker histone, suggesting that the higher-order structure is subject to secondary modulation by the associated histones.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allan J., Hartman P. G., Crane-Robinson C., Aviles F. X. The structure of histone H1 and its location in chromatin. Nature. 1980 Dec 25;288(5792):675–679. doi: 10.1038/288675a0. [DOI] [PubMed] [Google Scholar]
  2. Allan J., Staynov D. Z., Gould H. Reversible dissociation of linker histone from chromatin with preservation of internucleosomal repeat. Proc Natl Acad Sci U S A. 1980 Feb;77(2):885–889. doi: 10.1073/pnas.77.2.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aviles F. J., Danby S. E., Chapman G. E., Crane-Robinson C., Bradbury E. M. The conformation of histone H5 bound to DNA. Maintenance of the globular structure after binding. Biochim Biophys Acta. 1979 Jun 19;578(2):290–296. doi: 10.1016/0005-2795(79)90159-4. [DOI] [PubMed] [Google Scholar]
  4. Belyavsky A. V., Bavykin S. G., Goguadze E. G., Mirzabekov A. D. Primary organization of nucleosomes containing all five histones and DNA 175 and 165 base-pairs long. J Mol Biol. 1980 May 25;139(3):519–536. doi: 10.1016/0022-2836(80)90144-8. [DOI] [PubMed] [Google Scholar]
  5. Bonner W. M., Stedman J. D. Histone 1 is proximal to histone 2A and to A24. Proc Natl Acad Sci U S A. 1979 May;76(5):2190–2194. doi: 10.1073/pnas.76.5.2190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boulikas T., Wiseman J. M., Garrard W. T. Points of contact between histone H1 and the histone octamer. Proc Natl Acad Sci U S A. 1980 Jan;77(1):127–131. doi: 10.1073/pnas.77.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Butler P. J., Thomas J. O. Changes in chromatin folding in solution. J Mol Biol. 1980 Jul 15;140(4):505–529. doi: 10.1016/0022-2836(80)90268-5. [DOI] [PubMed] [Google Scholar]
  8. Camerini-Otero R. D., Sollner-Webb B., Felsenfeld G. The organization of histones and DNA in chromatin: evidence for an arginine-rich histone kernel. Cell. 1976 Jul;8(3):333–347. doi: 10.1016/0092-8674(76)90145-8. [DOI] [PubMed] [Google Scholar]
  9. Farmbrough D. M., Fujimura F., Bonner J. Quantitative distribution of histone components in the pea plant. Biochemistry. 1968 Feb;7(2):575–585. doi: 10.1021/bi00842a010. [DOI] [PubMed] [Google Scholar]
  10. Finch J. T., Klug A. Solenoidal model for superstructure in chromatin. Proc Natl Acad Sci U S A. 1976 Jun;73(6):1897–1901. doi: 10.1073/pnas.73.6.1897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Finch J. T., Lutter L. C., Rhodes D., Brown R. S., Rushton B., Levitt M., Klug A. Structure of nucleosome core particles of chromatin. Nature. 1977 Sep 1;269(5623):29–36. doi: 10.1038/269029a0. [DOI] [PubMed] [Google Scholar]
  12. Hohmann P. The H1 class of histone and diversity in chromosomal structure. Subcell Biochem. 1978;5:87–127. doi: 10.1007/978-1-4615-7942-7_2. [DOI] [PubMed] [Google Scholar]
  13. Hozier J., Renz M., Nehls P. The chromosome fiber: evidence for an ordered superstructure of nucleosomes. Chromosoma. 1977 Jul 18;62(4):301–317. doi: 10.1007/BF00327030. [DOI] [PubMed] [Google Scholar]
  14. Jaenicke L. A rapid micromethod for the determination of nitrogen and phosphate in biological material. Anal Biochem. 1974 Oct;61(2):623–627. doi: 10.1016/0003-2697(74)90429-1. [DOI] [PubMed] [Google Scholar]
  15. Johns E. W. The electrophoresis of histones in polyacrylamide gel and their quantitative determination. Biochem J. 1967 Jul;104(1):78–82. doi: 10.1042/bj1040078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kornberg R. D. Structure of chromatin. Annu Rev Biochem. 1977;46:931–954. doi: 10.1146/annurev.bi.46.070177.004435. [DOI] [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Lohr D., Tatchell K., Van Holde K. E. On the occurrence of nucleosome phasing in chromatin. Cell. 1977 Nov;12(3):829–836. doi: 10.1016/0092-8674(77)90281-1. [DOI] [PubMed] [Google Scholar]
  19. Lohr D., Van Holde K. E. Organization of spacer DNA in chromatin. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6326–6330. doi: 10.1073/pnas.76.12.6326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lohr D., Van Holde K. E. Yeast chromatin subunit structure. Science. 1975 Apr 11;188(4184):165–166. doi: 10.1126/science.1090006. [DOI] [PubMed] [Google Scholar]
  21. Lutter L. C. Precise location of DNase I cutting sites in the nucleosome core determined by high resolution gel electrophoresis. Nucleic Acids Res. 1979 Jan;6(1):41–56. doi: 10.1093/nar/6.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McGhee J. D., Rau D. C., Charney E., Felsenfeld G. Orientation of the nucleosome within the higher order structure of chromatin. Cell. 1980 Nov;22(1 Pt 1):87–96. doi: 10.1016/0092-8674(80)90157-9. [DOI] [PubMed] [Google Scholar]
  23. McKnight G. S. A colorimetric method for the determination of submicrogram quantities of protein. Anal Biochem. 1977 Mar;78(1):86–92. doi: 10.1016/0003-2697(77)90011-2. [DOI] [PubMed] [Google Scholar]
  24. Nelson P. P., Albright S. C., Wiseman J. M., Garrard W. T. Reassociation of histone H1 with nucleosomes. J Biol Chem. 1979 Nov 25;254(22):11751–11760. [PubMed] [Google Scholar]
  25. Noll M., Kornberg R. D. Action of micrococcal nuclease on chromatin and the location of histone H1. J Mol Biol. 1977 Jan 25;109(3):393–404. doi: 10.1016/s0022-2836(77)80019-3. [DOI] [PubMed] [Google Scholar]
  26. Olins A. L., Carlson R. D., Wright E. B., Olins D. E. Chromatin nu bodies: isolation, subfractionation and physical characterization. Nucleic Acids Res. 1976 Dec;3(12):3271–3291. doi: 10.1093/nar/3.12.3271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pehrson J., Cole R. D. Histone H10 accumulates in growth-inhibited cultured cells. Nature. 1980 May 1;285(5759):43–44. doi: 10.1038/285043a0. [DOI] [PubMed] [Google Scholar]
  28. Renz M., Day L. A. Transition from noncooperative to cooperative and selective binding of histone H1 to DNA. Biochemistry. 1976 Jul 27;15(15):3220–3228. doi: 10.1021/bi00660a010. [DOI] [PubMed] [Google Scholar]
  29. Renz M., Nehls P., Hozier J. Involvement of histone H1 in the organization of the chromosome fiber. Proc Natl Acad Sci U S A. 1977 May;74(5):1879–1883. doi: 10.1073/pnas.74.5.1879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Renz M. Preferential and cooperative binding of histone I to chromosomal mammalian DNA. Proc Natl Acad Sci U S A. 1975 Feb;72(2):733–736. doi: 10.1073/pnas.72.2.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Riley D., Weintraub H. Nucleosomal DNA is digested to repeats of 10 bases by exonuclease III. Cell. 1978 Feb;13(2):281–293. doi: 10.1016/0092-8674(78)90197-6. [DOI] [PubMed] [Google Scholar]
  32. Staynov D. Z. Thermal denaturation profiles and the structure of chromatin. Nature. 1976 Dec 9;264(5586):522–525. doi: 10.1038/264522a0. [DOI] [PubMed] [Google Scholar]
  33. Thoma F., Koller T., Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol. 1979 Nov;83(2 Pt 1):403–427. doi: 10.1083/jcb.83.2.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Urban M. K., Neelin J. M., Betz T. W. Correlation of chromatin composition with metabolic changes in nuclei of primitive erythroid cells from chicken embryos. Can J Biochem. 1980 Sep;58(9):726–731. doi: 10.1139/o80-102. [DOI] [PubMed] [Google Scholar]
  35. Weintraub H. The nucleosome repeat length increases during erythropoiesis in the chick. Nucleic Acids Res. 1978 Apr;5(4):1179–1188. doi: 10.1093/nar/5.4.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Weintraub H., Worcel A., Alberts B. A model for chromatin based upon two symmetrically paired half-nucleosomes. Cell. 1976 Nov;9(3):409–417. doi: 10.1016/0092-8674(76)90085-4. [DOI] [PubMed] [Google Scholar]
  37. Worcel A., Benyajati C. Higher order coiling of DNA in chromatin. Cell. 1977 Sep;12(1):83–100. doi: 10.1016/0092-8674(77)90187-8. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES